Research Article |
Corresponding author: Cyro de Luna-Dias ( cyroluna@gmail.com ) Academic editor: Angelica Crottini
© 2019 Cyro de Luna-Dias, Sergio P. de Carvalho-e-Silva.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Luna-Dias C, Carvalho-e-Silva SP (2019) Calls of Boana latistriata (Caramaschi & Cruz, 2004) (Amphibia, Anura, Hylidae), an endemic tree frog from the State of Minas Gerais, Brazil. ZooKeys 820: 83-94. https://doi.org/10.3897/zookeys.820.30711
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Bioacoustical data are useful for studying amphibians, especially their conservation, taxonomy, and evolution, among others. Of the 12 species of the Boana polytaenia clade, only B. buriti and B. latistriata have no published information about their advertisement calls. We recorded four males of B. latistriata in its type locality at Parque Nacional do Itatiaia, south-eastern Brazil. We used a Roland R26 digital recorder with a Sennheiser ME-67 microphone and analysed the recordings using the Raven Pro 1.5 software. We recorded two different types of calls (call A and call B). Both were composed of one pulsed note and presented a slightly ascending-descending frequency modulation. Call A was more frequent, having durations between 0.042 and 0.093 s with the dominant frequency ranging from 3375.0 to 3937.5 Hz, and was composed of 11 to 21 pulses separated by intervals that were not fully silent. Call B had durations between 0.711 and 1.610 s, with dominant frequency from 3281.2 to 3750.0 Hz, and was composed of 11 to 29 pulses separated by fully silent intervals. Among the B. polytaenia clade, the calls of B. latistriata are more similar to those of B. bandeirantes, B. beckeri, B. polytaenia, and B. aff. beckeri. The calls of B. latistriata differ from these species in its lower dominant frequency. Boana latistriata present a short, single-note call with a lower pulse period (call A) and a long call with higher pulse period (call B), which differ from the other species of the clade. The coefficients of variation for the various bioacoustical attributes were calculated within- and between-males and these have been discussed. We also report a fight event between two males of B. latistriata. This is the first report of a fight in members of the B. polytaenia clade.
Cophomantini , Boana pulchella species group, communication, bioacoustics, taxonomy
Vocalization plays an essential role during the reproductive period of anurans, being species-specific and constituting a pre-zygotic mechanism of reproductive isolation (
The Boana polytaenia clade is composed of 12 species of tree frogs with a striped dorsal pattern (
Boana latistriata was described from Brejo da Lapa, an artificial pond in the Parque Nacional do Itatiaia (PNI), Itamonte Municipality, State of Minas Gerais, Brazil (
Recordings were made at Brejo da Lapa (22.3589°S, 44.7372°W, 2140 m altitude) on 12 November 2014, from 20:30 to 23:00. Vocalizations from four males were recorded with a Roland R26 digital recorder and a Sennheiser ME-67 shotgun microphone positioned between 20 and 50 cm from the calling males. After the calls were recorded, the specimens were collected, anesthetised and euthanized with 5% lidocaine, fixed in 10% formaldehyde, and subsequently preserved in 70% ethanol. These have been deposited in the amphibian collection of the Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (
Recordings were made using 24 bits of resolution and 48 kHz sampling rate. Sound analyses were performed using the Raven Pro 1.5 software (
The following parameters were measured or calculated: call duration (CD), pulse duration (PD), pulse period (PP), interval between “call A” and “call B” (ABI), call dominant frequency (DF), call fundamental frequency (FF; measured through the “Peak Frequency” function of Raven Pro), number of visible harmonics (NH; integer multiples of the fundamental frequency), first pulse dominant frequency (FPDF), central pulse dominant frequency (CPDF, measured in the central pulse with higher dominant frequency), last pulse dominant frequency (LPDF), pulse rise time (RT; measured through the “Max Time” function of Raven Pro), proportion of pulse rise time in relation to pulse duration (RTR), and pulse number (PN). Measurements are given as a range, followed by mean and standard deviation (SD). For DF, FPDF, CPDF, LPDF, and PN, the mode (Mo; the most frequent value among the measurements) is also presented.
To determine the variation in the bioacoustical attributes, we calculated the within-individual coefficient of variation (CVw;
Males of B. latistriata called from dusk (about 18:00) to at least 02:00, perched on shrubs and grass, near or above the water. At the time of the recordings, we visually counted more than 20 males of B. latistriata and heard many more at a distance. During the fieldwork, the weather was rainy, air temperature between 12 and 14 °C, and humidity above 90%. Other amphibian species recorded at the site were Aplastodiscus albosignatus (Lutz & Lutz, 1938), Bokermannohyla gouveai (Peixoto & Cruz, 1992), Rhinella icterica (Spix, 1824), and Scinax duartei (Lutz, 1951).
We recorded two types of calls from the males of B. latistriata, herein called “call A” and “call B” (Fig.
Calls of Boana latistriata from its type locality. A Waveform and B spectrogram showing three instances of call A and one of call B emitted in sequence C waveform and D spectrogram of a call A, in detail, indicating seven visible harmonics numbered I to VII E waveform and F spectrogram of a call B, in detail. Images were obtained using Raven Pro 1.5 software. Spectrograms parameters: window type = Hann, size = 256 samples, overlap = 99%. Individual
Call A was composed of a single, short, pulsed note, with up to seven visible harmonics and duration from 0.042 to 0.093 s (mean = 0.073 s, SD = 0,012, n = 97 calls; Fig.
Call parameters for the call A of each recorded individual of Boana latistriata. Values are given as range, mean, standard deviation (SD), mode (Mo; when applicable) and sample number (n). Abbreviations: SVL, snout-vent length; CVw, within-individual coefficient of variation; CVb, between-individual coefficient of variation; CD, call duration; DF, dominant frequency; FF, fundamental frequency; PD, pulse duration; PP, pulse period; RT, pulse rise time; RTR, proportion of pulse rise time in relation to pulse duration; FPDF, first pulse dominant frequency; CPDF, central pulse dominant frequency; LPDF, last pulse dominant frequency; PN, pulse number. * All instances of call A of this individual presented some pulses fused in a pulsatile, which made it impossible to measure pulse parameters properly.
Parameters (Call A) | Individuals | Mean CVw | CVb | |||
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CD (s) | 0.066–0.089 | 0.067–0.078 | 0.077–0.094 | 0.042–0.078 | 7.7% | 16.2% |
mean = 0.080 | mean = 0.072 | mean = 0.084 | mean = 0.059 | |||
SD = 0.006; n = 31 | SD = 0.003; n = 15 | SD = 0.004; n = 22 | SD = 0.008; n = 29 | |||
CVw = 7.1% | CVw = 4.7% | CVw = 5.2% | CVw = 13.6% | |||
PD (s) (= PP) | 0.003–0.011 | 0.001–0.011 | 0.001–0.008 | * | 20.2% | 24.0% |
mean = 0.006 | mean = 0.005 | mean = 0.005 | ||||
SD = 0.001; n = 434 | SD = 0.001; n = 215 | SD = 0.001; n = 406 | ||||
CVw = 18.5% | CVw = 22.3% | CVw = 19.9% | ||||
PN | 11–16 | 11–17 | 17–21 | * | 8.4% | 15.5% |
mean = 13.9 | mean = 14.3 | mean = 18.5 | ||||
SD = 1.1 | SD = 1.5 | SD = 1.1 | ||||
Mo = 15; n = 31 | Mo = 15; n = 15 | Mo = 18; n = 22 | ||||
CVw = 8.1% | CVw = 10.8% | CVw = 6.2% | ||||
RT (s) | 0.001–0.004 | 0.001–0.005 | 0.001–0.003 | * | 25.7% | 25.0% |
mean = 0.002 | mean = 0.002 | mean = 0.002 | ||||
SD = 0.001; n = 434 | SD = 0.000; n = 215 | SD = 0.000; n = 406 | ||||
CVw = 23.9% | CVw = 24.4% | CVw = 28.8% | ||||
RTR (%) | 13.8–89.2 | 18.2–64.3 | 15.4–63.6 | * | 21.0% | 24.1% |
mean = 37.5 | mean = 37.4 | mean = 34.3 | ||||
SD = 11.5; n = 434 | SD = 5.6; n = 215 | SD = 5.9; n = 406 | ||||
CVw = 30.8% | CVw = 15.1% | CVw = 17.1% | ||||
DF (Hz) (= FF) | 3656.2–3937.5 | 3656.2–3843.8 | 3375.0–3656.2 | 3375.0–3562.5 | 2.1% | 4.6% |
mean = 3807.5 | mean = 3712.5 | mean = 3536.9 | mean = 3455.8 | |||
SD = 92.8 | SD = 69.1 | SD = 71.9 | SD = 69.6 | |||
Mo = 3750.0; n = 31 | Mo = 3656.2; n = 15 | Mo = 3562.5; n = 22 | Mo = 3468.8; n = 29 | |||
CVw = 2.5% | CVw = 1.9% | CVw = 2.0% | CVw = 2.0% | |||
FPDF (Hz) | 3375.0–3937.5 | 3562.5–3750.0 | 3000.0–3468.8 | * | 2.9% | 5.4% |
mean = 3668.3 | mean = 3618.7 | mean = 3328.1 | ||||
SD = 132.0 | SD = 69.1 | SD = 107.3 | ||||
Mo = 3656.2; n = 31 | Mo = 3562.5; n = 15 | Mo = 3375.0; n = 22 | ||||
CVw = 3.6% | CVw = 1.9% | CVw = 3.2% | ||||
CPDF (Hz) | 3656.2–4031.2 | 3656.2–3843.8 | 3375.0–3750.0 | * | 2.1% | 3.8% |
mean = 3861.9 | mean = 3737.5 | mean = 3588.1 | ||||
SD = 85.3 | SD = 69.7 | SD = 77.5 | ||||
Mo = 3843.8; n = 31 | Mo = 3750.0; n = 15 | Mo = 3562.5; n = 22 | ||||
CVw = 2.2% | CVw = 1.9% | CVw =2.2% | ||||
LPDF (Hz) | 3468.8–3843.8 | 3375.0–3468.8 | 3000.0–3468.8 | * | 2.5% | 6.3% |
mean = 3634.9 | mean = 3393.8 | mean = 3191.8 | ||||
SD = 95.9 | SD = 38.8 | SD = 124.4 | ||||
Mo = 3656.2; n = 31 | Mo = 3375.0; n = 15 | Mo = 3187.5; n = 22 | ||||
CVw = 2.6% | CVw = 1.1% | CVw = 3.9% |
Call B was composed of a single, long, pulsed note, with up to seven visible harmonics and call duration from 0.711 to 1.610 s (mean = 1.114 s, SD = 0.279, n = 37 calls; Fig.
Call parameters for the call B of each recorded individual of Boana latistriata. Values are given as range, mean, standard deviation (SD), mode (Mo; when applicable) and sample number (n). Abbreviations: SVL, snout-vent length; CVw, within-individual coefficient of variation; CVb, between-individual coefficient of variation; CD, call duration; DF, dominant frequency; FF, fundamental frequency; PD, pulse duration; PP, pulse period; RT, pulse rise time; RTR, proportion of pulse rise time in relation to pulse duration; FPDF, first pulse dominant frequency; CPDF, central pulse dominant frequency; LPDF, last pulse dominant frequency; PN, pulse number. Mode followed by an “-“ indicates that no value was more frequent than the others.
Parameters (Call B) | Individuals | Mean CVw | CVb | |||
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CD (s) | 1.030–1.234 | 1.301–1.476 | 1.564–1.610 | 0.711–0.894 | 4.5% | 25.1% |
mean = 1.130 | mean = 1.384 | mean = 1.577 | mean = 0.814 | |||
SD = 0.073; n = 12 | SD = 0.550; n = 8 | SD = 0.022; n = 4 | SD = 0.048; n = 14 | |||
CVw = 6.5% | CVw = 4.0% | CVw = 1.4% | CVw = 5.9% | |||
PD (s) | 0.003–0.012 | 0.001–0.010 | 0.003–0.010 | 0.004–0.013 | 16.9% | 21.2% |
mean = 0.007 | mean = 0.008 | mean = 0.008 | mean = 0.009 | |||
SD = 0.002; n = 214 | SD = 0.001; n = 170 | SD = 0.001; n = 106 | SD = 0.001; n = 192 | |||
CVw = 26.4% | CVw = 14.6% | CVw = 13.0% | CVw = 13.4% | |||
PP (s) | 0.009–0.152 | 0.024–0.166 | 0.024–0.121 | 0.026–0.196 | 38.5% | 41.4% |
mean = 0.066 | mean = 0.068 | mean = 0.062 | mean = 0.063 | |||
SD = 0.027; n = 203 | SD = 0.021; n = 162 | SD = 0.017; n = 102 | SD = 0.035; n = 178 | |||
CVw = 40.7% | CVw = 31.1% | CVw = 27.2% | CVw = 54.9% | |||
PN | 15–24 | 20–23 | 24–29 | 11–16 | 9.1% | 25.3% |
mean = 17.4 | mean = 21.3 | mean = 26.5 | mean = 13.7 | |||
SD = 2.3 | SD = 1.0 | SD = 2.4 | SD = 1.2 | |||
Mo = 17; n = 12 | Mo = 21; n = 8 | Mo = -; n = 4 | Mo = 14; n = 14 | |||
CVw = 13.5% | CVw = 4.9% | CVw = 9.0% | CVw = 8.8% | |||
RT (s) | 0.001–0.003 | 0.001–0.002 | 0.001–0.002 | 0.001–0.004 | 16.2% | 20.0% |
mean = 0.002 | mean = 0.002 | mean = 0.002 | mean = 0.002 | |||
SD = 0.001; n = 214 | SD = 0.000; n = 170 | SD = 0.000; n = 106 | SD = 0.000; n = 192 | |||
CVw = 24.2% | CVw = 12.7% | CVw = 14.7% | CVw = 13.1% | |||
RTR (%) | 18.8–51.6 | 14.8–50.0 | 16.3–50.0 | 14.2–44.2 | 16.5% | 21.2% |
mean = 31.9 | mean = 24.7 | mean = 25.5 | mean = 24.0 | |||
SD = 5.6; n = 214 | SD = 4.1; n = 170 | SD = 4.0; n = 106 | SD = 3.9; n = 192 | |||
CVw = 17.7% | CVw = 16.6% | CVw = 15.8% | CVw = 16.1% | |||
DF (Hz) (= FF) | 3281.2–3750.0 | 3375.0–3468.8 | 3468.8 | 3281.2–3375.0 | 1.5% | 4.1% |
mean = 3579.5 | mean = 3457.1 | min = max = mean = Mo | mean = 3301.3 | |||
SD = 137.9 | SD = 33.2 | SD = 0.0 | SD = 39.9 | |||
Mo = 3656.2; n = 12 | Mo = 3468.8; n = 8 | n = 4 | Mo = 3281.2; n = 14 | |||
CVw = 3.9% | CVw = 1.0% | CVw = 0.0% | CVw = 1.2% | |||
FPDF (Hz) | 3187.5–3562.5 | 3375.0–3468.8 | 3093.8–3187.5 | 3000.0–3375.0 | 2.4% | 4.2% |
mean = 3414.1 | mean = 3386.7 | mean = 3140.7 | mean = 3227.7 | |||
SD = 123.0 | SD = 33.2 | SD = 54.1 | SD = 102.1 | |||
Mo = 3562.5; n = 12 | Mo = 3375.0; n = 8 | Mo = 3187.5; n = 4 | Mo = 3281.2; n = 14 | |||
CVw = 3.6% | CVw = 1.0% | CVw = 1.7% | CVw = 3.2% | |||
CPDF (Hz) | 3562.5–3750.0 | 3468.8 | 3468.8 | 3187.5–3375.0 | 0.9% | 5.1% |
mean = 3703.1 | min = max = mean = Mo | min = max = mean = Mo | mean = 3293.7 | |||
SD = 63.2 | SD = 0.0 | SD = 0.0 | SD = 60.00 | |||
Mo = 3750.0; n = 12 | n = 8 | n = 4 | Mo = 3281.2; n = 14 | |||
CVw = 1.7% | CVw = 0.0% | CVw = 0.0% | CVw = 1.8% | |||
LPDF (Hz) | 2625.0–3656.2 | 3281.2–3468.8 | 2906.2–3468.8 | 3281.2–3468.8 | 4.7% | 5.8% |
mean = 3507.8 | mean = 3386.7 | mean = 3210.9 | mean = 3368.3 | |||
SD = 283.9 | SD = 60.1 | SD = 234.4 | SD = 57.8 | |||
Mo = 3562.5; n = 12 | Mo = 3375.0; n = 8 | Mo = -; n = 4 | Mo = 3375.0; n = 14 | |||
CVw = 8.1% | CVw = 1.8% | CVw = 7.3% | CVw = 1.7% |
In general, spectral parameters were static, while temporal parameters were dynamic. The most static parameter was the dominant frequency (mean CVw and CVb was 2.1% and 4.6% in call A and 1.5% and 4.1% in call B, respectively), while pulse period of call B was the most dynamic (CVw and CVb was 38.5% and 41.4%, respectively). Some parameters, including first pulse dominant frequency and last pulse dominant frequency in call A and central pulse dominant frequency and last pulse dominant frequency in call B, were intermediate in CVb, but static in CVw. All CVw and CVb values are shown in Tables
A fight event between two males of B. latistriata was witnessed during the recordings. A male (M1) was calling from the marginal vegetation, perched at approximately 20 cm from the water surface. A second male (M2) was calling from a floating shrub at approximately 40 cm from M1. Without any previous alteration on vocalization, M1 jumped over M2 and started the fight, both grasping and kicking. This first round lasted less than a second and resulted in M2 moving approximately 20 cm away. After a few seconds, M1 pursued M2, starting a second round of fighting, which lasted about the same time as the first one. After this, M2 swam to the other side of the pond, where it started calling a few minutes later. M1 returned to its original calling site and started calling again immediately. M1 was then recorded and collected, and is one of the individuals included in this study (
In this study, we describe two calls of B. latistriata and the coefficient of variation of its parameters. A fight event between two males is also reported. Although males of the species of the B. polytaenia clade frequently present dorsum marks that suggest fighting (C. Luna-Dias pers. comm.), this is the first published record of a fight for the clade. Although both intraspecific (
The calls of B. latistriata are similar to those of other species of the B. polytaenia clade. By presenting a shorter, single-note call with lower pulse period (call A), and a longer call with higher pulse period (call B), it resembles the calls from B. bandeirantes, B. beckeri, B. polytaenia, and B. aff. beckeri (
The calls of B. latistriata are distinguished from those of the four species whose calls are most similar to it by the lower dominant frequency of both calls A and B: 3375.0–3937.5 and 3281.2–3750.0 Hz, respectively, in B. latistriata (present study); 5340.2–5857.0 and 5340.2–5512.5 Hz, respectively, in B. bandeirantes (
Values of CV are linked to issues like recognition (at the species, population, and individual levels) and female preferences, and comparing those coefficients can be taxonomically informative (
Despite the similarities between the calls of the species of the B. polytaenia clade, different terminology used in call descriptions can lead to difficulties in comparing those descriptions if the terminology is not well explained. For example, structures of the call B herein defined as “pulses” were called as “notes” by
We thank Dr. Vinicius Guerra and an anonymous reviewer for their suggestions on the manuscript and Dr. Fabio Hepp for his help with the call structure and sidebands. This study was partially funded by grants 312606/2017-6 and 311156/2013-4 provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). CLD received a fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/CNPq).